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The Journal of Neuroscience, October 19, 2005, 25(42):9637-9648; doi:10.1523/JNEUROSCI.2932-05.2005

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Behavioral/Systems/Cognitive
Identification of a New Neuropeptide Precursor Reveals a Novel Source of Extrinsic Modulation in the Feeding System of Aplysia

Alex Proekt,¹ Ferdinand S. Vilim,¹ Vera Alexeeva,¹ Vladimir Brezina,¹ Allyson Friedman,¹ Jian Jing,¹ Lingjun Li,³ Yuriy Zhurov,¹ Jonathan V. Sweedler,² and Klaudiusz R. Weiss¹

¹Department of Neuroscience, Mount Sinai School of Medicine, New York, New York 10029, ²Department of Chemistry and Beckman Institute, University of Illinois, Urbana, Illinois 61801, and ³School of Pharmacy and Department of Chemistry, University of Wisconsin, Madison, Wisconsin 53705

The Aplysia feeding system is advantageous for investigating the role of neuropeptides in behavioral plasticity. One family of Aplysia neuropeptides is the myomodulins (MMs), originally purified from one of the feeding muscles, the accessory radula closer (ARC). However, two MMs, MMc and MMe, are not encoded on the only known MM gene. Here, we identify MM gene 2 (MMG2), which encodes MMc and MMe and four new neuropeptides. We use matrix-assisted laser desorption/ionization time-of-flight mass spectrometry to verify that these novel MMG2-derived peptides (MMG2-DPs), as well as MMc and MMe, are synthesized from the precursor. Using antibodies against the MMG2-DPs, we demonstrate that neuronal processes that stain for MMG2-DPs are found in the buccal ganglion, which contains the feeding network, and in the buccal musculature including the ARC muscle. Surprisingly, however, no immunostaining is observed in buccal neurons including the ARC motoneurons. In situ hybridization reveals only few MMG2-expressing neurons that are mostly located in the pedal ganglion. Using immunohistochemical and electrophysiological techniques, we demonstrate that some of these pedal neurons project to the buccal ganglion and are the likely source of the MMG2-DP innervation of the feeding network and musculature. We show that the MMG2-DPs are bioactive both centrally and peripherally: they bias egestive feeding programs toward ingestive ones, and they modulate ARC muscle contractions. The multiple actions of the MMG2-DPs suggest that these peptides play a broad role in behavioral plasticity and that the pedal-buccal projection neurons that express them are a novel source of extrinsic modulation of the feeding system of Aplysia.

Key words: MALDI mass spectrometry; cDNA cloning; neuropeptide processing; in situ hybridization; immunocytochemistry; feeding behavior

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Received July 15, 2005; revised August 31, 2005; accepted September 2, 2005.

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